Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
James Melrose
 -- 1288 2022-05-16 19:07:41 |
2 format correct
Conner Chen
Meta information modification 1288 2022-05-18 02:34:43 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Melrose, J. Application of HS Containing Biomatrices for Neural Repair. Encyclopedia. Available online: https://encyclopedia.pub/entry/22985 (accessed on 27 April 2024).
Melrose J. Application of HS Containing Biomatrices for Neural Repair. Encyclopedia. Available at: https://encyclopedia.pub/entry/22985. Accessed April 27, 2024.
Melrose, James. "Application of HS Containing Biomatrices for Neural Repair" Encyclopedia, https://encyclopedia.pub/entry/22985 (accessed April 27, 2024).
Melrose, J. (2022, May 16). Application of HS Containing Biomatrices for Neural Repair. In Encyclopedia. https://encyclopedia.pub/entry/22985
Melrose, James. "Application of HS Containing Biomatrices for Neural Repair." Encyclopedia. Web. 16 May, 2022.
Application of HS Containing Biomatrices for Neural Repair
Edit
This entry is adapted from the peer-reviewed paper 10.3390/ijms23095148

The fine structure (sulfation position and density) of the HS side chains of perlecan is an important regulatory determinant in the differentiation of pluripotent stem cells in the niche environment in neural tissues. Interaction of HS with growth factors (FGF-2) and morphogens (Wnt, SHh) is also essential for the long-term viability of recycling stem cells and the proliferation and differentiation of stem cells that have escaped from quiescent recycling and along with interactions with niche ECM components regulates the development of stem cell lineages that attain migratory properties facilitating their participation in neural repair processes. The expression of HS biosynthetic enzymes in the niche and tissue environments also have important roles in determining the fine structure of HS and how it exerts these effects spatially and temporally in tissue development and neural repair processes and also has roles in the determination of synaptic specificity, axonal guidance, synapse development and synapse function.

neural tissue repair extracellular matrix neural progenitor stem cells

1. Introduction

Hyaluronan (HA) is a major space-filling component of the CNS/PNS providing tissue hydration and a matrix for cell attachment and an environment conducive to cellular survival and cellular migration during CNS/PNS development [1][2][3]. HA also ensures specific niche environments, and ionic gradients are maintained in the 3D brain architecture to ensure optimal conditions for cellular activity. The brain extracellular matrix (ECM) is unusual in that it is dominated by glycosaminoglycans (GAGs), particularly HA, and it is one of the softest tissues in the human body. The immobilization of HA in the CNS ECM is critical to the optimal functional properties of the brain; however, HA is a soluble polymer, and it relies on interactions with proteoglycans (PGs), HA receptors and HA interactive glycoproteins for its immobilization in the CNS/PNS ECM [2]. HA is a component of both diffuse and condensed brain ECM structures known as perineuronal nets (PNNs), which protect neurons and are essential for the maintenance of optimal neural cellular activity [4]. HA is the only non-sulfated GAG and has a relatively simple repeat N-acetyl-glucosamine-D-glucuronic acid disaccharide structure. HA is highly interactive with the lectican PGs and HA-receptors and also influences cell migration in developing tissues [5]. High molecular weight HA is anti-inflammatory and mops up free radicals generated by inflammatory cells; thus, it counters the development of neuro-inflammation. The formation of HA-lectican aggregates (particularly HA-aggrecan aggregates) is critical to tissue hydration, brain volume, maintenance of cellular organization and micro-compartmentalization in the brain ECM. This provides niche and metabolite gradient environments that promote optimal cellular activities in the brain 3D environment. The importance of HA’s roles in brain tissues becomes apparent in tissues that display an HA deficiency. For example, brain tissues that are deficient in HA synthase-3 activity (Has3 KO) display frequent seizures and an epileptic phenotype [6][7].

2. Application of HS Containing Biomatrices for Neural Repair

Perlecan is also a major functional component of the stem cell niche and has many attributes with regard to tissue development and repair processes [8][9][10][11]. Perlecan is expressed in the basal neuroepithelium during neural development and is a crucial component of the neural niche [12][13]. Perlecan has multifunctional instructive properties [14] in developmental brain tissues [10][15] and promotes the proliferation and differentiation of neuroprogenitor stem cells in the sub-ventricular fractones through the sequestration of FGF-2 in the neural niche activating the Akt and Erk 1/2 cell signaling pathways [16]. The Wnt and ShH pathways also regulate stem cell proliferation, neurogenesis and neural network formation [17][18]. However, Wnt and Hedgehog proteins are relatively poorly soluble in aqueous media. Wnt and ShH bind to perlecan domain II, and this acts as a transport PG, aiding in the establishment of Wnt and ShH morphogen gradients in tissues that are important for tissue development [8]. The availability of recombinant perlecan domain I and domain V will allow investigations to be undertaken in the stimulation of neural repair processes in tissues [19][20][21][22] and in repair of the blood–brain barrier following ischemic stroke [23][24][25]. Further studies with perlecan in neural repair processes are expected in the future, and these offer exciting possibilities.

2.1. Harnessing Cell Instructive Properties of Perlecan’s HS Side Chains in Repair Biology

The fine structure (sulfation position and density) of the HS side chains of perlecan is an important regulatory determinant in the differentiation of pluripotent stem cells in the niche environment in neural tissues [26]. Interaction of HS with growth factors (FGF-2) and morphogens (Wnt, SHh) is also essential for the long-term viability of recycling stem cells and the proliferation and differentiation of stem cells that have escaped from quiescent recycling and along with interactions with niche ECM components regulates the development of stem cell lineages that attain migratory properties facilitating their participation in neural repair processes [11][23][27]. The expressions of HS biosynthetic enzymes in the niche and tissue environments also have important roles in determining the fine structure of HS and how it exerts these effects spatially and temporally in tissue development and neural repair processes and also has roles in the determination of synaptic specificity, axonal guidance, synapse development and synapse function [28]. Perlecan is an important regulatory cell instructive PG in the neural stem cell fractone [29]. The availability of recombinant perlecan domain I and domain V now makes it possible to incorporate these components into new generation bioscaffolds in neural repair strategies attempting to mimic the niche environment of native neural tissues. Such approaches used in combination with HA and neural progenitor stem cell preparations have a high probability of further improving on existing neural repair applications.
Collagen–HS porous scaffolds containing NSCs have been used to treat a rat model of traumatic brain injury, established using a controlled cortical impact [30]. Brain edema and cell apoptosis were significantly reduced, and motor and cognitive functions markedly improved using this procedure suggesting that porous collagen–HS scaffolds loaded with NSCs can improve neurological deficits in a rat model of traumatic brain injury [30]. Three-dimensional (3D) bioprinter-assembled collagen–HS scaffolds have also been used to treat controlled spinal cord injuries in rats [31]. The HS component of this scaffolding material crosslinks the collagen fibers, increasing its compression modulus and mechanical stability. This scaffold displays good biocompatibility with neurons co-administered within the scaffold. The HS component of this scaffold significantly improves the immobilization of bioavailable FGF-2, which promotes progenitor cell proliferation. A significant recovery in locomotor function and increased numbers of neurofilament positive cells were evident using this approach, suggesting that this matrix actively stimulates axonal guidance and neural repair processes. Porous bioscaffolds of chitosan–gelatin containing HA and/or HS have also been used in neural tissue engineering [32]. Such scaffolds contained highly interconnected pores ranging in size from 90 to 140 μm, and the scaffold had a porosity index of over 96%. Neural progenitor stem cells seeded into this matrix displayed adhesion, proliferation and multi-lineage differentiation in the 3D scaffold environment, indicating that this matrix may be useful in neural repair biology applications [32].

2.2. Development of Artificial Neural Stem Cell Niches

Significant improvements in bioscaffold microfabrication methodology has permitted the miniaturization of these platforms. Lithography and direct laser printing have been applied to prepare 2D patterns and 3D scaffolds to shape hydrogels and synthetic polymers to create niche-like structures for single neural cell culture [33]. Artificial laminin 3D neural stem cell niche-like structures have been developed to recapitulate the dynamic nature and some of the biological complexity of the neural stem cell niche and maintain laminin in a native conformation and orientation as found in the niche. These scaffolds support enhanced human NSC proliferation and neurite extension [34][35]. Stem cell niches are intricate spaces that provide specific chemical and biological environments that control stem cell fate [36]. Microdevices have been developed that have proved useful for the culture of NG108-15 neuroblastoma and human NPCs and represent a system amenable to modifications that promote these cellular activities for applications in neural repair biology [31][32][34].

References

  1. Delpech, B.; Delpech, A.; Brückner, G.; Girard, N.; Maingonnat, C. Hyaluronan and hyaluronectin in the nervous system. Ciba Found. Symp. 1989, 143, 208–285.
  2. Oohashi, T.; Edamatsu, M.; Bekku, Y.; Carulli, D. The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity. Exp. Neurol. 2015, 274 Pt B, 134–144.
  3. Suttkus, A.; Morawski, M.; Arendt, T. Protective Properties of Neural Extracellular Matrix. Mol. Neurobiol. 2016, 53, 73–82.
  4. Bosiacki, M.; Gąssowska-Dobrowolska, M.; Kojder, K.; Fabiańska, M.; Jeżewski, D.; Gutowska, I.; Lubkowska, A. Perineuronal Nets and Their Role in Synaptic Homeostasis. Int. J. Mol. Sci. 2019, 20, 4108.
  5. Peters, A.; Sherman, L.S. Diverse Roles for Hyaluronan and Hyaluronan Receptors in the Developing and Adult Nervous System. Int. J. Mol. Sci. 2020, 21, 5988.
  6. Arranz, A.; Perkins, K.L.; Irie, F.; Lewis, D.P.; Hrabe, J.; Xiao, F.; Itano, N.; Kimata, K.; Hrabetova, S.; Yamaguchi, Y. Hyaluronan deficiency due to Has3 knock-out causes altered neuronal activity and seizures via reduction in brain extracellular space. J. Neurosci. 2014, 34, 6164–6176.
  7. Perkins, K.; Arranz, A.M.; Yamaguchi, Y.; Hrabetova, S. Brain extracellular space, hyaluronan, and the prevention of epileptic seizures. Rev. Neurosci. 2017, 28, 869–892.
  8. Hayes, A.; Whitelock, J.; Melrose, J. Regulation of FGF-2, FGF-18 and Transcription Factor Activity by Perlecan in the Maturational Development of Transitional Rudiment and Growth Plate Cartilages and in the Maintenance of Permanent Cartilage Homeostasis. Int. J. Mol. Sci. 2022, 23, 1934.
  9. Hayes, A.; Farrugia, B.L.; Biose, I.J.; Bix, G.J.; Melrose, J. Perlecan, A Multi-Functional, Cell-Instructive, Matrix-Stabilizing Proteoglycan with Roles in Tissue Development Has Relevance to Connective Tissue Repair and Regeneration. Front. Cell Dev. Biol. 2022, 10, 856261.
  10. Girós, A.; Morante, J.; Gil-Sanz, C.; Fairén, A.; Costell, M. Perlecan controls neurogenesis in the developing telencephalon. BMC Dev. Biol. 2007, 7, 29.
  11. Arikawa-Hirasawa, E. Impact of the Heparan Sulfate Proteoglycan Perlecan on Human Disease and Health. Am. J. Physiol. Cell Physiol. 2022.
  12. Morrison, S.; Spradling, A.C. Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132, 598–611.
  13. Ford-Perriss, M.; Turner, K.; Guimond, S.; Apedaile, A.; Haubeck, H.D.; Turnbull, J.; Murphy, M. Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev. Dyn. 2003, 227, 170–184.
  14. Melrose, J. Perlecan, a modular instructive proteoglycan with diverse functional properties. Int. J. Biochem. Cell Biol. 2020, 128, 105849.
  15. Mashayekhi, F.; Sadeghi, M.; Rajaei, F. Induction of perlecan expression and neural cell proliferation by FGF-2 in the developing cerebral cortex: An in vivo study. J. Mol. Neurosci. 2011, 45, 87–93.
  16. Kerever, A.; Mercier, F.; Nonaka, R.; de Vega, S.; Oda, Y.; Zalc, B.; Okada, Y.; Hattori, N.; Yamada, Y.; Arikawa-Hirasawa, E. Perlecan is required for FGF-2 signaling in the neural stem cell niche. Stem Cell Res. 2014, 12, 492–505.
  17. De Luca, A.; Cerrato, V.; Fucà, E.; Parmigiani, E.; Buffo, A.; Leto, K. Sonic hedgehog patterning during cerebellar development. Cell. Mol. Life Sci. 2016, 73, 291–303.
  18. Ikeya, M.; Lee, S.M.; Johnson, J.E.; McMahon, A.P.; Takada, S. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 1997, 389, 966–970.
  19. Casper, C.; Yang, W.; Farach-Carson, M.C.; Rabolt, J.F. Coating electrospun collagen and gelatin fibers with perlecan domain I for increased growth factor binding. Biomacromolecules 2007, 8, 1116–1123.
  20. Jha, A.; Yang, W.; Kirn-Safran, C.B.; Farach-Carson, M.C.; Jia, X. Perlecan domain I-conjugated, hyaluronic acid-based hydrogel particles for enhanced chondrogenic differentiation via BMP-2 release. Biomaterials 2009, 30, 6964–6975.
  21. Srinivasan, P.; McCoy, S.Y.; Jha, A.K.; Yang, W.; Jia, X.; Farach-Carson, M.C.; Kirn-Safran, C.B. Injectable perlecan domain 1-hyaluronan microgels potentiate the cartilage repair effect of BMP2 in a murine model of early osteoarthritis. Biomed. Mater. 2012, 7, 024109.
  22. Yang, W.; Gomes, R.R.; Alicknavitch, M., Jr.; Farach-Carson, M.C.; Carson, D.D. Perlecan domain I promotes fibroblast growth factor 2 delivery in collagen I fibril scaffolds. Tissue Eng. 2005, 11, 76–89.
  23. Bix, G. Perlecan domain V therapy for stroke: A beacon of hope? ACS Chem. Neurosci. 2013, 4, 370–374.
  24. Marcelo, A.; Bix, G. Investigating the role of perlecan domain V in post-ischemic cerebral angiogenesis. Methods Mol. Biol. 2014, 1135, 331–341.
  25. Trout, A.; Kahle, M.P.; Roberts, J.M.; Marcelo, A.; de Hoog, L.; Boychuk, J.A.; Grupke, S.L.; Berretta, A.; Gowing, E.K.; Boychuk, C.R.; et al. Perlecan Domain-V Enhances Neurogenic Brain Repair After Stroke in Mice. Transl. Stroke Res. 2020, 12, 72–86.
  26. Yu, C.; Griffiths, L.R.; Haupt, L.M. Exploiting Heparan Sulfate Proteoglycans in Human Neurogenesis-Controlling Lineage Specification and Fate. Front. Integr. Neurosci. 2017, 11, 28.
  27. Kerever, A.; Schnack, J.; Vellinga, D.; Ichikawa, N.; Moon, C.; Arikawa-Hirasawa, E.; Efird, J.T.; Mercier, F. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 2007, 25, 2146–2157.
  28. Condomitti, G.; de Wit, J. Heparan Sulfate Proteoglycans as Emerging Players in Synaptic Specificity. Front. Mol. Neurosci. 2018, 11, 14.
  29. Zhang, P.; Lu, H.; Peixoto, R.T.; Pines, M.K.; Ge, Y.; Oku, S.; Siddiqui, T.J.; Xie, Y.; Wu, W.; Archer-Hartmann, S.; et al. Heparan Sulfate Organizes Neuronal Synapses through Neurexin Partnerships. Cell 2018, 174, 1450–1464.e23.
  30. Zhang, J.; Wang, R.J.; Chen, M.; Liu, X.Y.; Ma, K.; Xu, H.Y.; Deng, W.S.; Ye, Y.C.; Li, W.X.; Chen, X.Y.; et al. Collagen/heparan sulfate porous scaffolds loaded with neural stem cells improve neurological function in a rat model of traumatic brain injury. Neural Regen. Res. 2021, 16, 1068–1077.
  31. Chen, C.; Zhao, M.L.; Zhang, R.K.; Lu, G.; Zhao, C.Y.; Fu, F.; Sun, H.T.; Zhang, S.; Tu, Y.; Li, X.H. Collagen/heparin sulfate scaffolds fabricated by a 3D bioprinter improved mechanical properties and neurological function after spinal cord injury in rats. J. Biomed Mater. Res. A 2017, 105, 1324–1332.
  32. Guan, S.; Zhang, X.L.; Lin, X.M.; Liu, T.Q.; Ma, X.H.; Cui, Z.F. Chitosan/gelatin porous scaffolds containing hyaluronic acid and heparan sulfate for neural tissue engineering. J. Biomater. Sci. Polym. Ed. 2013, 24, 999–1014.
  33. Weißenbruch, K.; Lemma, E.D.; Hippler, M.; Bastmeyer, M. Micro-scaffolds as synthetic cell niches: Recent advances and challenges. Curr. Opin. Biotechnol. 2022, 73, 290–299.
  34. Barros, D.; Conde-Sousa, E.; Gonçalves, A.M.; Han, W.M.; García, A.J.; Amaral, I.F.; Pêgo, A.P. Engineering hydrogels with affinity-bound laminin as 3D neural stem cell culture systems. Biomater. Sci. 2019, 7, 5338–5349.
  35. Barros, D.; Amaral, I.F.; Pêgo, A.P. Laminin-Inspired Cell-Instructive Microenvironments for Neural Stem Cells. Biomacromolecules 2020, 21, 276–293.
  36. Buzanska, L.; Zychowicz, M.; Kinsner-Ovaskainen, A. Bioengineering of the Human Neural Stem Cell Niche: A Regulatory Environment for Cell Fate and Potential Target for Neurotoxicity. Probl. Cell Differ. 2018, 66, 207–230.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Cell & Tissue Engineering
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
James Melrose
View Times: 234
Revisions: 2 times (View History)
Update Date: 18 May 2022
Table of Contents
    1000/1000
    Hot Most Recent
    Feedback